This is a repository copy of Trace elements at the intersection of marine biological and geochemical evolution. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/107450/ Version: Accepted Version Article: Robbins, LJ, Lalonde, SV, Planavsky, NJ et al. (14 more authors) (2016) Trace elements at the intersection of marine biological and geochemical evolution. Earth-Science Reviews, 163. pp. 323-348. ISSN 0012-8252 https://doi.org/10.1016/j.earscirev.2016.10.013 © 2016, Elsevier. Licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/. Reuse Unless indicated otherwise, fulltext items are protected by copyright with all rights reserved. The copyright exception in section 29 of the Copyright, Designs and Patents Act 1988 allows the making of a single copy solely for the purpose of non-commercial research or private study within the limits of fair dealing. 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Konhauser PII: S0012-8252(16)30390-7 DOI: doi: 10.1016/j.earscirev.2016.10.013 Reference: EARTH 2339 To appear in: Earth Science Reviews Received date: 27 May 2016 Revised date: 11 October 2016 Accepted date: 30 October 2016 Please cite this article as: Robbins, Leslie J., Lalonde, Stefan V., Planavsky, Noah J., Partin, Camille A., Reinhard, Christopher T., Kendall, Brian, Scott, Clint, Hardisty, Dalton S., Gill, Benjamin C., Alessi, Daniel S., Dupont, Christopher L., Saito, Mak A., Crowe, Sean A., Poulton, Simon W., Bekker, Andrey, Lyons, Timothy W., Kon- hauser, Kurt O., Trace elements at the intersection of marine biological and geochemical evolution, Earth Science Reviews (2016), doi: 10.1016/j.earscirev.2016.10.013 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT Trace elements at the intersection of marine biological and geochemical evolution Leslie J. Robbins1, Stefan V. Lalonde2, Noah J. Planavsky3, Camille A. Partin4, Christopher T. Reinhard5, Brian Kendall6, Clint Scott7, Dalton S. Hardisty8, Benjamin C. Gill9, Daniel S. Alessi1, Christopher L. Dupont10, Mak A. Saito 11, Sean A. Crowe12, Simon W. Poulton13, Andrey Bekker8, Timothy W. Lyons8, Kurt O. Konhauser1 1Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB T6G 2E3, Canada 2European Institute for Marine Studies, CNRS-UMR6538 Laboratoire Domaines Océaniques, Technopôle Brest-Iroise, 29280 Plouzané, France 3Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA 4Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK S7N 5E2, Canada 5School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA 30332, USA 6Department of Earth and Environmental Sciences, University of Waterloo, Waterloo, ON, Canada 7United States Geological Survey, National Center, Reston, VA 20192, USA 8Department of Earth Sciences, University of California Riverside, Riverside, CA 92521, USA 9Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA 10Microbial and Environmental Genomics Group, J. Craig Venter Institute, La Jolla, CA 92121, USA 11Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA 12Department of Microbiology and Immunology and Department of Earth, Ocean, and Atmospheric Sciences,ACCEPTED University of British MANUSCRIPT Columbia, Vancouver, BC V6T 1Z3, Canada 13School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK *corresponding author: Leslie J. Robbins Department of Earth and Atmospheric Sciences, University of Alberta 1-26 University of Alberta, Edmonton, AB, Canada 1 ACCEPTED MANUSCRIPT Phone: 1-780-492-6532 Email: [email protected] Abstract Life requires a wide variety of bioessential trace elements to act as structural components and reactive centers in metalloenzymes. These requirements differ between organisms and have evolved over geological time, likely guided in some part by environmental conditions. Until recently, most of what was understood regarding trace element concentrations in the Precambrian oceans was inferred by extrapolation, geochemical modeling, and/or genomic studies. However, in the past decade, the increasing availability of trace element and isotopic data for sedimentary rocks of all ages have yielded new, and potentially more direct, insights into secular changes in seawater composition – and ultimately the evolution of the marine biosphere. Compiled records of many bioessential trace elements (including Ni, Mo, P, Zn, Co, Cr, Se, and I) provide new insight into how trace element abundance in Earth’s ancient oceans may have been linked to biological evolution. Several of these trace elements display redox-sensitive behavior, while others are redox-sensitive but not bioessential (e.g., Cr, U). Their temporal trends ACCEPTEDin sedimentary archives MANUSCRIPT provide useful constraints on changes in atmosphere-ocean redox conditions that are linked to biological evolution, for example, the activity of oxygen-producing, photosynthetic cyanobacteria. In this review, we summarize available Precambrian trace element proxy data, and discuss how temporal trends in the seawater concentrations of specific trace elements may be linked to the evolution of both simple and complex life. We also examine several biologically relevant and/or redox-sensitive trace elements that have yet to be fully examined in the 2 ACCEPTED MANUSCRIPT sedimentary rock record (e.g., Cu, Cd, W) and suggest several directions for future studies. Key words: Iron formations, black shales, eukaryotes, prokaryotes, evolution, trace elements, biolimitation, Precambrian 1 Introduction The trace elements utilized in metalloenzymes today are commonly thought to reflect, to some degree, the availability of trace elements in ancient seawater when those metalloenzymes first evolved. It was first realized in 1988 that trace metal availability exerted significant control over phytoplankton productivity (Martin and Fitzwater, 1988). In the early 1990’s, as part of the first edition of their seminal book, Frausto da Silva and Williams (2001) suggested that a cell’s trace element inventory was directly related to the conditions under which the host organism evolved. This profound suggestion, along with increasing recognition that trace element availability exerted control on primary productivity and other metabolic activities, stimulated a new generation of studies examining trace ACCEPTEDelement use and limitation MANUSCRIPT in marine microorganisms (e.g., Sunda and Huntsman, 1995; Saito et al., 2002). Indeed, Sunda and Huntsman (1995) arguably provide the first experimental evidence for absolute Co requirements in cyanobacteria. The idea that an organism’s trace element requirements are dependent on the environment in which it evolved stems from the simple observation that the biogeochemical cycling of many bioessential elements can vary dramatically under different aqueous conditions (see also Williams and Rickaby, 2012). In this light, some 3 ACCEPTED MANUSCRIPT trace element limitations observed in the modern ocean might be thought of as an evolutionary legacy of earlier life adapted to more replete conditions. This idea is easily illustrated with iron, which is the most common metal co-factor and a limiting micronutrient in large regions of the oceans today, especially high-nutrient low chlorophyll (HNLC) regions (for reviews see Zahariev et al., 2008; Moore et al., 2013). By contrast, iron would have been much more abundant in surface waters on a more reducing Earth when basic microbial metabolic machinery was being established (e.g., Poulton and Canfield, 2011; David and Alm, 2011). Thus, modern iron demand can be thought of as an evolutionary relict, stemming from the emergence of lineages under ancient environmental conditions of relative Fe abundance. The leading alternative to this model is that organismal elemental requirements are driven almost entirely by utility, i.e., cellular function, with shifts in biological requirements decoupled from corresponding environmental abundances (Scott et al., 2013; Robbins et al., 2013; Stüeken et al.,